Crystal structures and kinetics of monofunctional proline dehydrogenase provide insight into substrate recognition and conformational changes associated with flavin reduction and product release

Biochemistry

Volumn 51, Issue 50, 2012, Pages 10099-10108

  Luo, Min ^a   Arentson, Benjamin W ^b   Srivastava, Dhiraj ^a   Becker, Donald F ^b   Tanner, John J ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BULK SOLVENTS; CATALYTIC EFFICIENCIES; CONFORMATIONAL CHANGE; CONFORMATIONAL SELECTION; DEINOCOCCUS RADIODURANS; ELECTRON ACCEPTOR; ENZYME-INHIBITOR COMPLEX; FLAVOENZYMES; ION PAIRS; MONOFUNCTIONAL; OXIDIZED STATE; PRODUCT RELEASE; PROLINE DEHYDROGENASE; REDUCED-STATE; STRUCTURAL CHANGE; SUBSTRATE AFFINITY; SUBSTRATE RECOGNITION;

CARBOXYLATION; CATALYSIS; CRANKSHAFTS;

AMINO ACIDS;

FLAVOPROTEIN; PROLINE DEHYDROGENASE; QUERCETIN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DEINOCOCCUS RADIODURANS; ELECTRON; ENZYME CONFORMATION; ENZYME STRUCTURE; GENE MUTATION; HYDROGEN BOND; KINETICS; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; FLAVIN-ADENINE DINUCLEOTIDE; FLAVINS; FURANS; KINETICS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; PROLINE OXIDASE;

DEINOCOCCUS; DEINOCOCCUS RADIODURANS;

EID: 84871285122     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301312f     Document Type: Article

References (36)

1. Adams, E. and Frank, L. (1980) Metabolism of proline and the hydroxyprolines Annu. Rev. Biochem. 49, 1005-1061
2. Tanner, J. J. (2008) Structural biology of proline catabolism Amino Acids 35, 719-730
3. Singh, R. K. and Tanner, J. J. (2012) Unique Structural Features and Sequence Motifs of Proline Utilization A (PutA) Front. Biosci. 17, 556-568
4. Phang, J. M. (1985) The regulatory functions of proline and pyrroline-5-carboxylic acid Curr. Top. Cell. Regul. 25, 92-132
5. Phang, J. M., Donald, S. P., Pandhare, J., and Liu, Y. (2008) The metabolism of proline, a stress substrate, modulates carcinogenic pathways Amino Acids 35, 681-690
6. Donald, S. P., Sun, X. Y., Hu, C. A., Yu, J., Mei, J. M., Valle, D., and Phang, J. M. (2001) Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species Cancer Res. 61, 1810-1815
7. Hu, C. A., Donald, S. P., Yu, J., Lin, W. W., Liu, Z., Steel, G., Obie, C., Valle, D., and Phang, J. M. (2007) Overexpression of proline oxidase induces proline-dependent and mitochondria-mediated apoptosis Mol. Cell. Biochem. 295, 85-92
8. Liu, Y., Borchert, G. L., Surazynski, A., Hu, C. A., and Phang, J. M. (2006) Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: The role of ROS/superoxides, NFAT and MEK/ERK signaling Oncogene 25, 5640-5647
9. Pandhare, J., Cooper, S. K., and Phang, J. M. (2006) Proline oxidase, a proapoptotic gene, is induced by troglitazone: Evidence for both peroxisome proliferator-activated receptor γ-dependent and -independent mechanisms J. Biol. Chem. 281, 2044-2052
10. Cooper, S. K., Pandhare, J., Donald, S. P., and Phang, J. M. (2008) A novel function for hydroxyproline oxidase in apoptosis through generation of reactive oxygen species J. Biol. Chem. 283, 10485-10492
11. Phang, J. M., Pandhare, J., and Liu, Y. (2008) The metabolism of proline as microenvironmental stress substrate J. Nutr. 138, 2008S-2015S
12. Phang, J. M., Pandhare, J., Zabirnyk, O., and Liu, Y. (2008) PPARγ and Proline Oxidase in Cancer PPAR Res. 2008, 542694
13. Liu, Y., Borchert, G. L., Donald, S. P., Diwan, B. A., Anver, M., and Phang, J. M. (2009) Proline oxidase functions as a mitochondrial tumor suppressor in human cancers Cancer Res. 69, 6414-6422
14. Liu, Y., Borchert, G. L., Donald, S. P., Surazynski, A., Hu, C. A., Weydert, C. J., Oberley, L. W., and Phang, J. M. (2005) MnSOD inhibits proline oxidase-induced apoptosis in colorectal cancer cells Carcinogenesis 26, 1335-1342
15. Phang, J. M., Hu, C. A., and Valle, D. (2001) Disorders of proline and hydroxyproline metabolism. In Metabolic and molecular basis of inherited disease (Scriver, C. R., Beaudet, A. L., Sly, W. S., and Valle, D., Eds.) pp 1821-1838, McGraw-Hill, New York.
16. Willis, A., Bender, H. U., Steel, G., and Valle, D. (2008) PRODH variants and risk for schizophrenia Amino Acids 35, 673-679
17. Lee, Y. H., Nadaraia, S., Gu, D., Becker, D. F., and Tanner, J. J. (2003) Structure of the proline dehydrogenase domain of the multifunctional PutA flavoprotein Nat. Struct. Biol. 10, 109-114
18. Zhang, M., White, T. A., Schuermann, J. P., Baban, B. A., Becker, D. F., and Tanner, J. J. (2004) Structures of the Escherichia coli PutA proline dehydrogenase domain in complex with competitive inhibitors Biochemistry 43, 12539-12548
19. Ostrander, E. L., Larson, J. D., Schuermann, J. P., and Tanner, J. J. (2009) A conserved active site tyrosine residue of proline dehydrogenase helps enforce the preference for proline over hydroxyproline as the substrate Biochemistry 48, 951-959
20. Srivastava, D., Schuermann, J. P., White, T. A., Krishnan, N., Sanyal, N., Hura, G. L., Tan, A., Henzl, M. T., Becker, D. F., and Tanner, J. J. (2010) Crystal structure of the bifunctional proline utilization A flavoenzyme from Bradyrhizobium japonicum Proc. Natl. Acad. Sci. U.S.A. 107, 2878-2883
21. White, T. A., Krishnan, N., Becker, D. F., and Tanner, J. J. (2007) Structure and kinetics of monofunctional proline dehydrogenase from Thermus thermophilus J. Biol. Chem. 282, 14316-14327
22. Kabsch, W. (2010) XDS Acta Crystallogr. D66, 125-132
23. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr. D62, 72-82
24. Vagin, A. and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025
25. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
26. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
27. Moxley, M. A., Tanner, J. J., and Becker, D. F. (2011) Steady-state kinetic mechanism of the proline:ubiquinone oxidoreductase activity of proline utilization A (PutA) from Escherichia coli Arch. Biochem. Biophys. 516, 113-120
28. Zhang, W., Zhang, M., Zhu, W., Zhou, Y., Wanduragala, S., Rewinkel, D., Tanner, J. J., and Becker, D. F. (2007) Redox-induced changes in flavin structure and roles of flavin N(5) and the ribityl 2′-OH group in regulating PutA-membrane binding Biochemistry 46, 483-491
29. White, T. A., Johnson, W. H., Jr., Whitman, C. P., and Tanner, J. J. (2008) Structural basis for the inactivation of Thermus thermophilus proline dehydrogenase by N-propargylglycine Biochemistry 47, 5573-5580
30. Srivastava, D., Zhu, W., Johnson, W. H., Jr., Whitman, C. P., Becker, D. F., and Tanner, J. J. (2010) The structure of the proline utilization a proline dehydrogenase domain inactivated by N-propargylglycine provides insight into conformational changes induced by substrate binding and flavin reduction Biochemistry 49, 560-569
31. Becker, D. F., Zhu, W., and Moxley, M. A. (2011) Flavin redox switching of protein functions Antioxid. Redox Signaling 14, 1079-1091
32. Moxley, M. A. and Becker, D. F. (2012) Rapid reaction kinetics of proline dehydrogenase in the multifunctional proline utilization A protein Biochemistry 51, 511-520
33. Grant, B. J., Gorfe, A. A., and McCammon, J. A. (2010) Large conformational changes in proteins: Signaling and other functions Curr. Opin. Struct. Biol. 20, 142-147
34. Engh, R. A. and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure refinement Acta Crystallogr. A47, 392-400
35. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry:, ψ and Cβ deviation Proteins 50, 437-450
36. DeLano, W. L. (2002) The PyMOL User's Manual, DeLano Scientific, San Carlos, CA.